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ORI GIN AL PA PER
The status of the freshwater pearl mussel Margaritiferamargaritifera in Scotland: extent of change since 1990s,threats and management implications
Peter Cosgrove1 • Jon Watt2 • Lee Hastie3 • Iain Sime4 •
Donald Shields1 • Cameron Cosgrove1 • Lorna Brown2 •
Isabel Isherwood2 • Miguel Bao3
Received: 1 February 2016 / Revised: 8 June 2016 / Accepted: 11 July 2016� Springer Science+Business Media Dordrecht 2016
Abstract All known rivers in Scotland with recent records of freshwater pearl mussels
Margaritifera margaritifera were surveyed in 2013–2015 using a standard methodology.
Freshwater pearl mussel populations were classed as: (i) apparently extinct in 11 rivers, (ii)
not successfully recruiting in 44 rivers, and (iii) evidence of recent successful recruitment
in 71 rivers. On a regional basis, a high proportion of extant populations were located in
North and West Scotland. In all regions extant populations were characterised by low pearl
mussel densities, with 97 of 115 extant Scottish populations defined as ‘rare’ (0.1–0.9
mussels per 1 m 2) or ‘scarce’ (1.0–9.9 mussels per 1 m 2). Only 18 Scottish rivers now
hold pearl mussel populations in densities that are considered to be ‘common’ (10–19.9
mussels per 1 m 2) or ‘abundant’ ([20 mussels per 1 m 2). Based on survey evidence, the
number of apparently extinct pearl mussel populations in Scottish rivers is now 73. The
decline is particularly pronounced in the West Highlands and Western Isles strongholds.
The key threats are: (i) pearl fishing, (ii) low host fish densities, (iii) pollution/water
quality, (iv) climate change and habitat loss, (v) hydrological management/river engi-
neering and (vi) ‘other factors’, such as non-native invasive species. Over the last
100 years this endangered species has been lost from much of its former Holarctic range.
Scotland’s extant M. margaritifera populations continue to be of international importance,
but their continued decline since the first national survey in 1998 is of great concern.
Keywords Endangered species � Population decline � Aquatic conservation � Rivers
Communicated by Angus Jackson.
& Peter [email protected]
1 Alba Ecology Ltd, Coilintra House, Grantown on Spey, Moray PH26 3EN, UK
2 Waterside Ecology, Druimindarroch, Arisaig, Inverness-shire PH39 4NR, UK
3 School of Natural and Computing Sciences, University of Aberdeen, Tillydrone Avenue,Aberdeen AB24 2TZ, UK
4 Scottish Natural Heritage, Great Glen House, Leachkin Road, Inverness IV3 8NW, UK
123
Biodivers ConservDOI 10.1007/s10531-016-1180-0
Introduction
The freshwater pearl mussel Margaritifera margaritifera is threatened throughout its
Holarctic range and is classified by the International Union for the Conservation of Nature
(IUCN) as Critically Endangered in Europe (Moorkens 2011) having declined by 95 % in
central Europe (Degerman et al. 2009). The largest remaining populations in Scotland,
Ireland, Norway, Finland, Sweden and northwest Russia are of international importance
(Cosgrove et al. 2014). The freshwater mussels (Unionacea) are among the most imperilled
group of species in the world and have attracted much concern from conservationists
because of the important role they play in freshwater ecosystems (Strayer et al. 2004).
To date there has been only one national survey of freshwater pearl mussels in Scotland.
This Scottish Natural Heritage (SNH) funded research took place between 1996 and 1999,
and produced the first overall picture of the species’ status in Scotland. One hundred and
fifty-five rivers with historical pearl mussel records in the previous 100 years were sur-
veyed for the presence of freshwater pearl mussels and the results reported (Cosgrove et al.
2000a). Evidence of recent juvenile recruitment was found in only 52 rivers (34 % of the
total surveyed) and these populations were classified as ‘functional’ on the basis of their
continued ability to reproduce successfully. Approximately two-thirds of the 155 rivers
occupied previously (101 rivers) were assessed as ‘extinct’ (no mussels present) or con-
sidered ‘functionally extinct’ (only adult mussels present with no evidence of juvenile
recruitment in the previous ca. 15 years) (Cosgrove et al. 2000a).
The current survey was commissioned by SNH to update the 1996–1999 information,
assess the present status of surviving M. margaritifera populations and determine changes
in abundance, distribution and threats across Scotland. The results are intended to con-
tribute to the Scottish Biodiversity Surveillance Strategy and to allow Scotland and the UK
to adequately report on the status of M. margaritifera to the European Union. A number of
new (previously unsurveyed) populations have been discovered since the first national
survey was conducted and these too were included in the current survey.
Freshwater pearl mussel habitat requirements
The freshwater pearl mussel has a complex life-cycle, which makes it vulnerable to a
number of threats. The species is found in fast flowing unpolluted rivers and streams, with
detailed studies on Scottish freshwater pearl mussel populations suggesting that optimum
water depths of 0.3–0.4 m and optimum current velocities of 0.25–0.75 ms-1 at inter-
mediate water levels are most suitable (Hastie et al. 2000a). River bed substratum char-
acteristics appear to be the best physical parameters for describing freshwater pearl mussel
habitat in Scotland. Freshwater pearl mussels prefer stable cobble/boulder dominated
substrate with some fine substrate that allows the mussels to burrow (Cosgrove et al.
2000b; Fig. 1). Adult and juvenile mussels tend to have similar habitat preferences,
although adults are found over a wider range of physical conditions and juveniles appear to
be more exacting in their habits requiring fine stable sediments, particularly clean sand and
gravel (Hastie et al. 2000a). Of specific importance to freshwater pearl mussel survival are
levels of silt, suspended solids, biochemical oxygen demand, calcium and chemical
compounds generally associated with enrichment (eutrophication) i.e. nitrate and phos-
phate (Bauer 1983; Moorkens 2000; Degerman et al. 2009, 2013).
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Freshwater pearl mussel host requirements
Freshwater pearl mussels have a short parasitic larval phase on the gills of suitable native
salmonid host fish. The larvae (glochidia) of M. margaritifera are host-specific and can
only complete their development on Atlantic salmon Salmo salar or brown/sea trout Salmo
trutta. Usually juvenile fish (fry and parr) are utilised (Young and Williams 1984). The
presence of freshwater pearl mussels in any river therefore depends on salmonid host fish
availability and there is some adaptive matching between species/races of fish and mussels
(Geist et al. 2006). This complexity illustrates the many potential threats and pressures that
operate on M. margaritifera and its habitat.
Objectives
The main objectives of the present survey were:
• To survey all known watercourses in Scotland with extant freshwater pearl mussel
populations and report on their current status.
• To identify positive and negative factors that may be contributing to the present
condition of populations in each watercourse.
Methods
The current survey was carried out in two separate phases. The first was a desk study
conducted by SNH that collated all known records of rivers containing freshwater pearl
mussel using previous survey reports. This desk assessment then provided the basis for a
standardised survey of almost all rivers in Scotland with freshwater pearl mussel records.
This was carried out in 2013–2015. A small number of rivers that had already recently
been surveyed (post 2010) were not resurveyed, but their results are reported here as part of
this updated assessment of the status of M. margaritifera in Scotland.
Fig. 1 Freshwater pearl mussel substrate habitat, West Highlands
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For the purpose of this study (and to repeat methods used in 1996–1999) a river was
defined as a named watercourse on 1:25,000 Ordnance Survey maps. If, for example, a
named tributary containing pearl mussels joined the main pearl mussel watercourse, then
for the purpose of reporting and analysis both named watercourses were considered sep-
arate ‘pearl mussel rivers’.
Site selection
The survey was based on a list of rivers provided by SNH. It included the majority of
Scottish watercourses with known populations of freshwater pearl mussels (those rivers
recorded with pearl mussels in the first national survey and new populations discovered
since then). It also included a small number of rivers where there were recent anecdotal
reports of freshwater pearl mussels, but for which no confirmed records existed.
As a consequence of the threat posed by illegal pearl fishing, the names and locations of
specific pearl mussel rivers are treated as confidential and are not reported here, but are
instead provided geographically, based on the hydrological regions defined by Maitland
et al. (1994) (Fig. 2).
Fig. 2 Scottish Hydrological Regions (after Maitland et al. 1994)
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The Scottish rivers within this survey varied considerably in size from the largest, which
averaged ca. 70 m in width and 2 m in depth (Fig. 3) to the smallest, which averaged ca.
2 m in width and 0.2 m in depth (Fig. 4).
Selection of specific locations to be visited in each river
The first national pearl mussel survey in 1996–1999 involved a significant element of
searching, as the locations of pearl mussel populations were unknown (Cosgrove et al.
2000a). Selection of original transect locations in the first national survey was focussed on
river reaches known, or believed, to have previously held pearl mussels. These were often
where pearl fishers had been active and so other search areas were also chosen from a map
study. Cosgrove et al. (2000a) reported that an attempt was made to include all main sub-
divisions of the rivers.
Fig. 3 Typical large-sized Scottish pearl mussel river, Grampian
Fig. 4 Typical small-sized Scottish pearl mussel river, West Highlands
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As the current survey was largely intended to be a repeat of the 1996–1999 survey, it
was clear that, where possible, the same transect locations should be revisited. However,
were the current survey limited only to revisiting original transect locations this may not
reflect the current status or distribution of the freshwater pearl mussel population in a
catchment. This is for three main reasons. Firstly, research conducted by Hastie et al.
(2001) in Scotland demonstrated that pearl mussels move and mussel habitats change over
time, especially in relation to significant floods, which have occurred with greater fre-
quency in recent years (Cosgrove et al. 2012a). Revisiting only the original transect
locations would provide an assessment of status in formerly suitable locations. These are
not necessarily the best or most representative current locations. Secondly, the first survey
spent on average one day per river surveying at least three representative areas. This
typically meant surveying in the lower, middle and upper river reaches. In several rivers
however, some remote reaches were not surveyed at all. The element of seeking out further
suitable habitat and areas populated by mussels, which was a key part of the first survey,
was incorporated into the current survey as well as revisiting the previous transect loca-
tions. Thirdly, knowledge of freshwater pearl mussel distribution in some rivers has
increased since 1996–1999 and it was judged important to incorporate new sites and areas
where these were known—particularly where they extended mussel range beyond that
identified in 1996–1999 or where their omission might be expected to alter the reported
population status (e.g. known recruiting mussel beds). In practice, this meant that surveyors
had to balance repeating all 1996–1999 transects against omitting one or more to (i) ex-
plore new areas of potential mussel habitat, or (ii) survey transects where significant
numbers of mussels had been identified more recently.
As a result of the above considerations, not all previous transects were repeated in every
river, but most were. Generally a larger number of transects were completed in 2013–2015
than in 1996–1999. The approach taken is likely to have resulted in a more complete
picture of current status than would have resulted from an exact repeat of 1996–1999
survey locations.
Survey methodology for live mussels
The standard Scottish field survey protocol for freshwater pearl mussels was used to assess
the distribution, age structure, and size of populations in each river (based on Young et al.
2003). The standard survey methodology, conducted by teams of highly experienced and
licensed surveyors, involved the following:
• Searches were made using a glass-bottomed viewing bucket, under favourable
conditions (i.e. bright light, clear water and a low flow regime) and in water sufficiently
shallow for safe wading.
• Searches were made in an upstream direction, checking possible and potentially
suitable areas of habitat (e.g. in the shelter of boulders or over-hanging banks).
• If no mussels were found, the search was continued until a range of potentially
suitable locations had been searched within the area selected. An area was considered
to not support pearl mussels after it had been searched for approximately two person
hours or until no further suitable habitat could be identified.
• If mussels were found, a transect 50 m long by 1 m wide was laid out so as to traverse
the main area of suitable habitat at a location. All mussels in a 1 m wide ‘corridor’ were
counted.
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• At 10, 20, 30, 40 and 50 m along each transect, 1 m 9 1 m quadrats were laid on the
substrate. Within these quadrats all visible M. margaritifera were counted, removed
and measured along their maximum dimension to the nearest 1 mm using dial callipers
(note, juvenile mussels defined as B65 mm in length). All loose stones and debris were
then displaced in order to reveal any hidden mussels and to search for any juveniles.
• If it became clear that more than 250 visible mussels were present in the transect, a full
count as above was abandoned. Instead, five 1 9 1 m quadrats were placed at 10, 20,
30, 40 and 50 m. Each was surveyed as for the standard placing of quadrats. An
estimated total for the whole transect was extrapolated from the visible numbers in the
five 1 9 1 m quadrats.
• All live mussels were returned to the river in the approximate locations where they
were found.
Standard field sheets were completed for each transect. Transect locations were
recorded using 12-figure grid references generated by hand-held GPS at the downstream
end of transects. Transect locations were photographed and sketched in order to aid future
site identification.
Standard criteria for describing the relative abundance of M. margaritiferapopulations
Mussel relative abundance in each survey transect is expressed using absolute numbers
counted and standardised abundance codes/terms. The abundance classification (Table 1)
is based on the number of live mussels found in a standard 50 m 9 1 m transect. These
relative abundance terms are based on visible, i.e. unburied mussels, and were also used in
the 1996–1999 survey.
A single population classification was provided for each watercourse surveyed. Popu-
lation status was categorised following Cosgrove et al. (2012a), based on the presence or
absence of adult and juvenile mussels across all transects. The categories are directly
comparable with those used by Cosgrove et al. (2000a) in the first national survey although
different terminology was used (Table 2). The change in terminology was prompted by the
Table 1 The mussel abundance classifications for 50 m transects
Mussels in 50 m transect (N) Visible mussel density per 1 m2 Relative abundance code Term used
C1000 [20 A Abundant
500–999 10–19.9 B Common
50–499 1–9.9 C Scarce
1–49 0.1–0.9 D Rare
0 0 E Absent
Table 2 Pearl mussel population status terminology used for watercourses, 1996–1999 and 2013–2015
Survey findings Status term used 1996–1999 Status term used 2013–2015
Mussels absent Extinct Apparently extinct
Mussels present, juveniles absent Functionally extinct Not successfully recruiting
Mussels present, juveniles present Functional Recent successful recruitment
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findings of Hastie et al. (2011), showing that small, adult only apparently non-recruiting
populations retained capacity for reproduction.
Temporal trends in population status
Population status (Table 2) is used as the basis for comparison when comparing current
survey results with those from the first national survey. A number of rivers were included
in the current survey that were not assessed or known of during the first national survey.
Where more than two consecutive and comparable surveys have taken place, these rivers
are included in analyses of temporal trends.
Eighteen watercourses (15 %) with extant M. margaritifera populations were not sur-
veyed during 2013–2015 because recent survey data already existed (defined as 2010 or
later). These watercourses were included in regional and national analyses, using the most
recent survey data (post 2010) to determine current status. Mussel populations in each
watercourse for which there were baseline and current/recent data were defined as
declined, unchanged or improved. Decline was defined as an observed change in popu-
lation status, from ‘not successfully recruiting’ to ‘apparently extinct’ or from ‘recent
successful recruitment’ to either of the other two status categories. Improvement was
defined as any change in the opposite direction. One new and previously unknown pearl
mussel watercourse is included that was discovered after completion of the 2013–2015
SNH funded study.
Threat assessment
Where evidence was available, surveyors identified apparent threats to each river M.
margaritifera population. In order to present these regionally and nationally, threats were
categorised following the methods of Cosgrove et al. (2000a), who identified five broad
categories of threat: (i) pearl fishing, (ii) pollution/water quality, (iii) hydrological man-
agement/river engineering (iv) ‘other threats’ and (v) unknown. A new sixth category—
low host fish density or host fish decline—was defined and used for the current survey.
This threat was identified using one or more of the following criteria: (i) recent survey data
showing host fish density of less than 0.2 host fish per square metre in watercourse (after
Zuiganov et al. 1994); (ii) reported declines of adult stocks of salmon or trout (using catch
or fish counter data) suggesting potential stock collapse.
Results
The current status of M. margaritifera in Scotland
A total of 126 watercourses were surveyed as part of the current study. Fifty-eight rivers
that were surveyed in the first national survey, but where pearl mussels were determined to
be ‘extinct’ in 1996–1999 were not resurveyed in the current survey.
Based on current survey data, there were 115 Scottish watercourses with extant pop-
ulations of freshwater pearl mussels (Table 3). Seventy-one (56 %) of the rivers included
in the current survey showed some sign of recent recruitment. This represents 62 % of the
watercourses with extant populations. Based on current data, a total of 44 rivers (ap-
proximately one-third of river populations) were not recruiting. Eleven apparent river
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extinctions were recorded since the first national survey. These and other changes are
considered further below.
Unsurprisingly the current regional status of extant populations largely matches that
found during the first national survey, with a high proportion of sites located in the north
and west of Scotland, including the Western Isles (Fig. 5). Many of the sites with evidence
of recent recruitment were in the north and west of Scotland but high levels of recruitment
were also recorded in some large east coast Grampian rivers.
An analysis was conducted of the relative abundance classifications across regional
areas and nationally (Table 4). For this analysis, the abundance code used for each river
was that of the highest scoring 50 m transect on the river. In all regions extant pearl mussel
populations were dominated by relative abundance codes C and D (scarce-rare). Less than
a third of pearl mussel populations in any region held relative abundance codes A and B
(abundant-common). Despite there being 19 known mussel rivers in the Western Isles no
transect exceeded abundance code C and three were assessed as apparently extinct since
the first national survey. Nationally, 97 of the 115 extant Scottish populations (84 %) were
classified as scarce-rare. In other words, only 18 of Scotland’s rivers (16 % of those
surveyed) now hold pearl mussel populations in densities that are considered to be com-
mon-abundant.
Figure 6 provides a breakdown of changes in population status by hydrological region.
Of the 105 rivers for which current and previous baseline data are both available, mussel
population status remained unchanged in 75 watercourses. A further 21 rivers showed
evidence of decline while only nine showed some improvement. Improvements outnum-
bered declines only in the NE Highland region.
Of the eleven instances of apparent recent extinction (Table 4), ten occurred in rivers
where no evidence of recruitment was found in the first national survey, and only one river
previously defined as ‘functional’ (based on the presence of a single juvenile in first
national survey) has become extinct. No particular regional trends are apparent, with
extinctions in both east and west coast watercourses. In addition to the extinctions, ten
rivers were recorded as declining due to failure of recruitment since they were first sur-
veyed. Recent recruitment failure was recorded in all regions with the exception of Orkney
and Shetland where there is only one known M. margaritifera population.
Apparent improvements in status arising from a record of recent recruitment occurred in
nine watercourses (of which six were included in the first national survey and three were
surveyed in the intervening period). The improved classifications of three of these were the
result of finding a single large juvenile mussel in each river (65, 64 and 60 mm respec-
tively), so these improved classifications may be considered weak or tenuous at best. The
Table 3 Current Scottish freshwater pearl mussel status classification in surveyed watercourses 2013–2015
Region Recruiting Not recruiting Extinct Total rivers Total extant rivers
SW Scotland 0 3 0 3 3
Grampian 10 4 4 18 14
NE Highlands 12 11 1 24 23
Orkney and Shetland 0 1 0 1 1
W Highlands 38 20 3 61 58
W Isles 11 5 3 19 16
Scotland 71 44 11 126 115
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Recent recruitment No recent recruitment
N=1N=16
N=14
N=3
N=58
N=23
Fig. 5 The current status of M. margaritifera populations in Scottish Hydrological Regions
Table 4 The relative abundance status of freshwater pearl mussel populations in Scottish HydrologicalRegions (proportion of extant regional populations only in parenthesis)
Hydrological region Maximum abundance classification per transect All rivers (n)
A B C D E
SW Scotland 0 0 1 (33.3) 2 (66.7) 0 3
Grampian 1 (7.1) 1 (7.1) 4 (28.6) 8 (57.1) 4 18
NE Highlands 4 (17.4) 2 (8.7) 5 (21.7) 12 (52.2) 1 24
Orkney and Shetland 0 0 0 1 (100) 0 1
West Highlands 6 (10.3) 4 (6.9) 26 (44.8) 22 (37.9) 3 61
Western Isles 0 0 6 (37.5) 10 (62.5) 3 19
Scotland 11 7 42 55 11 126
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original classification of one river (located in NE Highland) was based on a single 50 m
transect and so the apparent improvement in mussel population status from this water-
course is likely to have been an artefact of increased sampling effort in the current survey,
where five transects were undertaken in 2014.
Threats
In order to assess current threats and trends, it is important to consider changes that have
occurred between the first and second national surveys (a period of 15 years). Using and
expanding upon the categories listed by Cosgrove et al. (2000a), this report assesses
specific threats, based on evidence of their occurrence at all the rivers surveyed in
2013–2015. Table 5 summarises threats identified in pearl mussel rivers in each hydro-
logical region and these are considered further in the Discussion. The apparently recently
extinct watercourses are included, as the extinctions have presumably occurred due to
recent or ongoing pressures.
Discussion
Overall status of Scottish freshwater pearl mussel populations
Cosgrove et al. (2000a) reported that the pearl mussel population in 58 of the 155 rivers
surveyed between 1996 and 1999 were extinct. These extinct rivers were not resurveyed in
the current study and it is assumed that the former populations in these watercourses
remain extinct, based on a sub-set being resurveyed for potential reintroduction in 2007
(ERA/Cosgrove and Hastie 2007).
Therefore, of the 126 known pearl mussel river populations, the evidence from 2013 to
2015 suggests that:
• Apparently extinct = 11 rivers;
0
5
10
15
20
25
30
35
40
SWScotland
Grampian NEHighlands
Orkney &Shetland
WestHighlands
WesternIsles
Num
ber o
f wat
erco
urse
s
Declined
Unchanged
Improved
Fig. 6 Trends in pearl mussel status by Scottish Hydrological Region (data from rivers with 2 sets of datafor comparative purposes)
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• Not successfully recruiting = 44 rivers with no evidence of recent successful juvenile
recruitment; and
• Recent successful recruitment = 71 rivers with evidence of successful juvenile
recruitment.
It should be borne in mind that Cosgrove et al. (2000a) reported that pearl mussels had
already become extinct from 58 Scottish rivers occupied in the previous 100 years.
Between the first national survey and the current survey, an additional four former pearl
mussel rivers were surveyed and populations were found to be extinct. Thus, combined
survey evidence from surveys since 1996 indicates that the number of apparently extinct
Scottish pearl mussel rivers known is now 73.
Based on the findings of the first national survey, Cosgrove et al. (2000a) provided
estimates of historical extinction (i.e. disappearance) rates for Scottish M. margaritifera
populations. It was apparent that, in Scotland, M. margaritifera declined throughout the
twentieth century, and that the annual rate of population extinction accelerated during the
latter 30 years of the last century, from an estimated 0.5 extinctions/year during the period
1901–1970 to an estimated 2 extinctions/year during the period 1971–2000 (Cosgrove
et al. 2000a). The results of the current survey indicate that the extinction rate may have
slowed since then. Although this reduction in rate is to be welcomed, a further 15 popu-
lation extinctions in Scotland during the past 15 years represents a significant loss to one of
the remaining global strongholds of M. margaritifera. To continue conserving the species
every effort must be made to arrest any further losses.
Threats to Scottish freshwater pearl mussel populations
Pearl fishing
During the first national survey 99 % of Scottish pearl mussel populations were considered
to have been affected by pearl fishing (Cosgrove et al. 2000a). Illegal pearl fishing is still a
threat to all Scottish pearl mussel populations. Annual pearl fishing mortality levels as high
Table 5 Specific threats identified in pearl mussel rivers in each Hydrological Region (percentage inparenthesis)
Region Threat category
Rivers(N)
Pearlfishing
Pollution/waterquality
Hydro’impact/riverengineering
Host fish Climatechange/riverbed instability
Other
SW Scotland 3 2 (66.7) 3 (100) 0 (0) 0 (0) 0 (0) 0 (0)
Grampian 18 7 (38.9) 6 (33.3) 8 (44.4) 1 (5.6) 4 (22.2) 1 (5.6)
NE Highlands 24 5 (20.8) 6 (25) 10 (41.7) 0 (0) 9 (37.5) 4 (16.7)
Orkney andShetland
1 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 1 (100)
WestHighlands
61 24 (39.3) 14 (23) 5 (8.2) 28 (45.9) 8 (13.1) 4 (6.6)
Western Isles 19 6 (31.6) 2 (10.5) 0 (0) 5 (26.3) 5 (26.3) 3 (15.8)
Scotland 126 44 31 23 34 26 13
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as 5–10 % (representing 25–50 % of total mortality) were estimated for a sample of
exploited Scottish M. margaritifera populations (Hastie 2006). These levels are clearly
unsustainable in the long term, and support the view of Cosgrove et al. (2000a), that
historical pearl fishing pressure was a major cause of extinction in a number of Scottish M.
margaritifera populations. However, to provide meaningful up to date information on pearl
fishing incidents and potential impacts, pearl fishing is listed as a direct current
threat/pressure only on those rivers where there has been direct evidence of recent pearl
fishing activity (post 1999).
Despite being fully protected since 1998, large numbers of freshwater pearl mussels
have been illegally killed each year since then (Cosgrove et al. 2012b). The most recent
statistics in the Scottish wildlife crime annual report (Table 6; Scottish Government 2015)
show that between two and 12 confirmed incidents of wildlife crime affecting pearl
mussels were recorded annually between 2009 and 2014. These incidents have been
reported across the Scottish mainland and from several of the Hebridean Islands. The
consequence of this pressure on the conservation of the species is such that freshwater
pearl mussels remain a UK wildlife crime priority.
Pearl-fishing offences are hard to detect for a number of practical and logistical reasons.
Given the remote distribution of the majority of remaining pearl mussel populations,
offences tend to occur in places seldom visited by many people. If evidence is left behind,
it can often be years before it is found and reported, severely reducing the likelihood of
perpetrators being apprehended (Cosgrove et al. 2012b). Furthermore, few people know
what pearl-fishing signs to look for and where to find them. Finally, we have seen evidence
of pearl-fishers changing their behaviour and deliberately hiding evidence of offences
(discarded shells), so that populations of pearl mussels just ‘disappear’ from an area for no
apparent reason (pers. obs.).
The complete disappearance of mussels in this manner means that assessment of pearl
fishing impact can become more speculative, because direct evidential basis of decline or
loss in such cases is lacking. There is no evidence to suggest that natural predation of pearl
mussels causes significant mortality. Indeed, such events are rather rare and opportunistic
in nature, resulting in the death of very small numbers of mussels in an identifiable manner
(Cosgrove et al. 2007).
Given the difficulties in identifying and recording pearl fishing incidents, it is likely that
the number of rivers where evidence of illegal pearl fishing activity has been recorded is an
underestimate of the number of actual incidents since the first national survey. Never-
theless, based on the data collected from the four sources outlined above, there is direct
evidence of pearl fishing since the 1998 ban (e.g. Fig. 7) in a minimum of 34.9 % of 126
Scottish rivers that were included in the analysis (Table 5). No particularly striking
regional trends emerge, the proportion of affected rivers being largely independent of
geography at the scale used for analysis. The individual river accounts do not throw much
Table 6 Suspected criminalincidents on freshwater pearlmussels in Scotland 2009–2014(Scottish Government 2015)
Financial year Number of incidents
2009–2010 10
2010–2011 12
2011–2012 4
2012–2013 2
2013–2014 8
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additional light on which rivers are most likely to be threatened; accessible sites and
remote sites both showing evidence of impact. However, a high proportion of designated
sites, which have been surveyed much more than undesignated sites, have reported pearl
fishing kills since 1998. Whether this is simply a reflection of survey and reporting effort
being greater on designated sites or reflects a real focus by illegal pearl fishers on some of
largest extant (and publicised) watercourses is unknown. It is clear that effort to reduce this
threat via current media campaigns, increased intelligence gathering and improved
policing remain necessary and a conservation priority.
Pollution/water quality
Pollution and poor water quality are known to kill and adversely affect pearl mussels (e.g.
Bauer 1988; Moorkens 2000; Young et al. 2001; Degerman et al. 2009). Given that this
survey did not measure water quality, the issue is only identified for pearl mussel rivers
where there was direct evidence or evidence of impact (e.g. dead in situ mussels, plumes of
silt or pollution from point sources, excessive algal growth, sewage fungus etc.). Former
pearl mussel rivers where pollution would have wiped out entire populations were sur-
veyed in the first national survey and were not revisited again in the current survey. Thus,
only on-going or recent incidents involving pollution and/or poor water quality are
reported. Based on the data collected by surveyors during the current survey, there is
evidence that 24.6 % of 126 pearl mussel river populations having been affected by
pollution or poor water quality between 1999 and 2015 (Table 5).
Care needs to be taken interpreting these data and further analyses may be warranted. In
a number of rivers where pollution was recorded it was highly localised (e.g. a single septic
tank outfall impacting on one mussel bed). Such localised impact may not affect the overall
status of a large, dispersed mussel population, but may threaten a very small, restricted one.
Water quality effects that are more diffuse or whose impact is more widespread are of
greater concern. Perhaps surprisingly, 23 % of West Highlands watercourses were judged
Fig. 7 Despite full legal protection, illegal pearl fishing kills are reported annually. This pile of shells waspart of an estimated pearl fishing kill of[1000 mussels, West Highlands, 2014
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to be threatened to some degree by water quality concerns despite the region’s relative
remoteness. In addition to the toxic impact already mentioned above, the three main factors
resulting in water quality concerns in West Highlands were forestry, agriculture (mainly
trampling by cattle leading to runoff and associated siltation) and the presence of dense
algal growth. Surveyors also recorded greatly increased algal growth in two watercourses
after one large intentional fire (known in the UK as ‘muirburn’) and one large potentially
unintentional fire. Recent research has documented chemical changes, increased suspended
solids and detrimental impacts on stream biota in catchments subject to regular muirburn
(Ramchunder et al. 2013).
Agricultural effects on water quality were identified as a concern in some rivers in
Grampian, NE Highlands and SW Scotland, a factor that has already led to the extinction
of many pearl mussel populations in these regions (Cosgrove et al. 2000a). Deliberate or
accidental poisoning of streams, such as occurred in two watercourses, are also a cause for
real concern, adversely impacting both on pearl mussels and their host salmonids.
Hydrological management/river engineering
Hydrological management, including river engineering, dams, water abstractions, and
channel modifications has historically been responsible for the decline and extinction of a
number of Scottish pearl mussel populations and potentially remains a significant threat
(Cosgrove and Hastie 2001). Based on the data collected during the current survey, there is
evidence of a minimum of 18.3 % of pearl mussel river populations having been adversely
affected by hydrological management or river engineering between 1999 and 2015
(Table 5). This includes eight sites where historic changes to hydrology, mainly by con-
struction of major dams and barriers for hydroelectric generation, are likely to have an
ongoing impact on flow regimes and sediment budgets.
There is a degree of interplay between river engineering and water quality, especially
during the construction phase of engineering projects when siltation or other forms of
pollution may occur. Siltation associated with the construction of hydro-electric schemes
has been identified on two extant pearl mussel rivers, one leading to the first successful
prosecution for damaging pearl mussels in Scotland (Scottish Government 2013). Rigorous
monitoring of water quality for construction projects in pearl mussel streams requires ‘eyes
on the river’ and the employment of suitably accredited, trained and independent Eco-
logical or Environmental Clerks of Work is recommended wherever such projects take
place to ensure compliance with planning conditions and pollution prevention measures.
Host fish
Low numbers of host salmonid stocks have been identified as a potential threat to pearl
mussels in Scotland (Hastie and Cosgrove 2001). The issue can be both generic (as with the
threat of pearl fishing across all populations) and specific with locally low densities of host
salmonids (e.g. Sinclair 2011). This is further complicated by the apparent issue of host
specificity, where some pearl mussel populations appear to utilise only one species of fish;
Atlantic salmon or trout, and not both (Hastie and Young 2001). Potential low host fish
density has been listed as a threat where evidence of an apparent lack of host fish (e.g. few/
none seen) was observed or where specific electric fishing data have been identified
showing low fish abundance. However, it is important to recognise that a more general
pressure may be occurring in some areas, such as the widespread sea trout stock decline in
West Highlands (e.g. Walker 1994; Butler and Watt 2003; Butler and Walker 2006).
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Actual or potential low host fish densities are identified as a concern on 34 watercourses
(27 %) included in the survey (Table 5). There is a very clear and striking regional pattern,
with the greatest threat in West Highlands and Western Isles. Twenty-eight rivers in West
Highlands (45.9 % of the total) were classified as being threatened by low host fish
numbers. In 18 of these watercourses, the classification is backed up by electric fishing data
on juvenile salmonid densities (e.g. Sinclair 2011; Argyll Fisheries Trust 2007; Wester
Ross Fisheries Trust 2012; West Sutherland Fisheries Trust 2015). In 15 West Highland
rivers sea trout and/or salmon stock collapses have been reported and documented by local
fisheries organisation or in published literature (e.g. Argyll Fisheries Trust 2009; Waterside
Ecology 2010).1 In our view, these numbers are likely to be conservative as few data are
available for many smaller watercourses without commercially valuable fisheries. Data
from the Western Isles are scarce as fewer electric fishing or catch data for individual
watercourses are publicly accessible. Nevertheless five (26.3 %) rivers in the Western Isles
were considered at threat based on electric fishing data (Argyll Fisheries Trust 2004;
Sinclair 2011; Waterside Ecology 2010; Watt 2006). It is likely that low fish numbers may
be a significant concern and linked to the lack of recruitment in several other pearl mussel
populations in the West Highland and Western Isles regions for which no fish population
data have been identified. Sea trout stock collapses have occurred in a number of rivers in
SW Scotland (Ayrshire River Trust 2009) and, dependent on host species, may represent a
further significant threat to mussels in this region.
Ongoing research suggests that a number of (but not all) pearl mussel populations in
NW Scotland may be trout adapted (e.g. Baum 2015; Hastie et al. 2011), suggesting that
low juvenile trout numbers may be a major concern in the core part of the extant Scottish
pearl mussel range. Host fish concerns feature less heavily in eastern catchments, where
salmonid densities are typically higher (Godfrey 2006). This is consistent with contrasting
historic data trends in sea trout numbers on the two sides of the country (see e.g. Anon
1995; Scottish Government 2009). More recent analyses conducted by Scottish Govern-
ment (2015) also indicate ongoing concern over salmon stocks in the West Highlands and
Western Isles, where most require management action due to their predicted failure to meet
conservation targets.
Climate change and habitat loss
The threat posed to pearl mussels by climate change has been recognised for many years
(e.g. Hastie et al. 2003). During recent work to identify potential reintroduction sites for
pearl mussels in Scotland, it became apparent that several rivers appeared to have changed
in character (Cosgrove et al. 2012a). In particular the riverbed habitat in some former pearl
mussel rivers had become predominantly unstable and this habitat loss has been attributed
to increased spate events consistent with the changing climate in Scotland. Such change
was particularly pronounced in rivers without headwater lochs to ameliorate very rapid
changes in water discharge during spates (Cosgrove et al. 2012a). In the present survey
climate change was identified as a potential threat where there was reason to believe that
the habitat has changed and become unstable recently. It is recognised that this is a very
difficult and subjective assessment because no empirical, systematic substrate stability data
has been collected on pearl mussel rivers. Climate effects were only included when loss of
previously suitable habitat had clearly occurred (i.e. no suitable habitat at former transect
1 Many stock collapses have been reported on a named river by river basis so cannot be referenced herein asthis would identify vulnerable pearl mussel watercourses.
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locations and adjacent areas) or where professional judgement indicated a high probability
of ongoing loss of habitat (extreme scouring, bank collapse, etc.).
Climate change and increasing substrate mobility was identified as a probable threat in
26 (20.6 %) watercourses surveyed (Table 5). Climate induced change may be one of the
most difficult threats to ameliorate through medium-term management actions and it may
only be possible to make generic recommendations in this regard. For example, expanding
native riparian woodland cover in catchments denuded of tree cover and blocking moor-
land/farmland/forestry drainage ditches are warranted, as well as actions to restore natural
geomorphological processes, which can help sustain sediment transport and maintain pearl
mussel and host fish habitat.
Other factors
Approximately 10 % of surveyed streams were judged to be threatened from sources not
covered by the broad categories set out above (Table 5). These ‘other’ factors range from
non-native introductions e.g. Ranunculus spp. (Laughton et al. 2008) to over-shading by
conifers, caused by former poor forestry management. Whilst other non-native species
introductions (such as signal crayfish Pacifastacus leniusculus and zebra mussel Dreissena
polymorpha) potentially threaten many rivers, none of these yet directly threaten extant
Scottish pearl mussel populations and so have been excluded from the threat analysis.
Nevertheless, signal crayfish are now present in catchments adjacent to globally important
pearl mussel rivers (Spey Fishery Board 2014), and have recently been recorded within
catchments supporting pearl mussels (but not yet in the watercourses hosting pearl mussels
themselves).
Conclusion
Whilst it is encouraging that just over half of Scotland’s extant freshwater pearl mussel
populations show some signs of recruitment, the overall trend since the first national survey
is one of continuing decline. This has come about due to the apparent extinction of some
populations and recruitment failure in others. Furthermore, the trends identified above may
mask weak or failing recruitment in many rivers, since the coarse analyses conducted are
based only on the presence or absence of juvenile pearl mussels. Such analyses do not
distinguish between the presence of one large juvenile, which would suggest very weak
recruitment, and many juveniles of varied sizes, which would suggest strong and regular
recruitment. In fact it is clear from the data from individual rivers that weak recruitment is
an ongoing threat to many existing Scottish M. margaritifera populations. For a number of
reasons pearl mussel sample sizes varied considerably between rivers and this may have
affected the results, particularly in small or sparse populations where few mussels were
found or measured. Nonetheless, this was also true of the first national survey and the
overall trends are almost certainly genuine.
In the medium term, mitigation effort to enhance pearl mussel recruitment levels should
be targeted in those catchments where recruitment is absent or weak, through actions such
as host infection initiatives or host fish conservation measures. Protecting mussel popu-
lations from direct threats such as pearl fishing must also continue and the implementation
of site specific actions should be encouraged and supported where possible. These should
focus on implementing measures to protect and restore suitable habitat for juvenile pearl
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mussels in particular. Cosgrove et al. (2000a) highlighted that a distinctive and worrying
feature of remaining M. margaritifera populations across its range was a general lack of
juveniles (e.g. Bauer 1986; Zuiganov et al. 1994; Chesney and Oliver 1998; Cosgrove et al.
2000a; Hastie et al. 2000b; Osterling et al. 2010). Hence any locations or areas of rivers
with signs of recent juvenile recruitment are of particular importance in terms of the long-
term viability of a pearl mussel population. The results of the present study support and
reinforce this emphasis and practitioners should make conservation efforts in such areas a
priority in Scotland and elsewhere. Even in the absence of specific autoecological infor-
mation, clear ‘no regrets’ conservation measures such as riparian woodland restoration,
blocking of forestry, moorland or agricultural drainage ditches and reductions in diffuse
pollution should continue. In the longer term, identifying and ameliorating the particular
causal factors underlying weak or failed recruitment remains the most pressing conser-
vation priority for this species in Scotland.
Scotland’s extant freshwater pearl mussel populations continue to be of international
importance but their continued decline since the first national survey is of great concern.
The decline is particularly pronounced in West Highlands and Western Isles strongholds,
compared to eastern rivers in Grampian and NE Highlands. Over the last 100 years the
species has been lost from much of its former range and new and continued action from a
range of stakeholders is required to secure the future of M. margaritifera in Scotland.
Acknowledgments We are grateful to SNH for providing funds to help finance this study as part of itsresearch and monitoring programme. Forestry Commission Scotland funded some additional studies andallowed their data to be used for the present survey, which we appreciate. We are very grateful to manyfarmers, fishery managers, estate managers, charitable foundations and their staff (too numerous to mention)for their logistical support and encouragement during 3 years of fieldwork. The authors would personallylike to thank the following people for their direct help and support: Kjersti Birkeland, Stephen Corcoran,Jackie Farquhar, Alison Gibb, Tim Goucher, David Jarrett, Kenny Kortland, Neil McInnes, Amy Mitchell,Julie Murray, Robert Potter, April Socrates, Hilary Swift and Edwin Third.
Compliance with ethical standards
Conflicts of interest P. Cosgrove, J. Watt, L. Hastie, D. Shields, C. Cosgrove, L. Brown, I. Isherwood andM. Bao received conservation research funding from SNH to undertake the Scottish national freshwaterpearl mussel survey reported here. I. Sime was the SNH Project Manager for the Scottish national freshwaterpearl mussel survey and undertook the desk study element of this work.
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